Abstract
Background
Chinese jujube (Ziziphus jujuba Mill.) is a non-climacteric fruit; however, the underlying mechanism of ripening and the role of abscisic acid involved in this process are not yet understood for this species.
Results
In the present study, a positive correlation between dynamic changes in endogenous ABA and the onset of jujube ripening was determined. Transcript analyses suggested that the expression balance among genes encoding nine-cis-epoxycarotenoid dioxygenase (ZjNCED3), ABA-8′-hydroxylase (ZjCYP707A2), and beta-glucosidase (ZjBG4, ZjBG5, ZjBG8, and ZjBG9) has an important role in maintaining ABA accumulation, while the expression of a receptor (ZjPYL8), protein phosphatase 2C (ZjPP2C4–8), and sucrose nonfermenting 1-related protein kinase 2 (ZjSnRK2–2 and ZjSnRK2–5) is important in regulating fruit sensitivity to ABA applications. In addition, white mature ‘Dongzao’ fruit were harvested and treated with 50 mg L− 1 ABA or 50 mg L− 1 nordihydroguaiaretic acid (NDGA) to explore the role of ABA in jujube fruit ripening. By comparative transcriptome analyses, 1103 and 505 genes were differentially expressed in response to ABA and NDGA applications on the 1st day after treatment, respectively. These DEGs were associated with photosynthesis, secondary, lipid, cell wall, and starch and sugar metabolic processes, suggesting the involvement of ABA in modulating jujube fruit ripening. Moreover, ABA also exhibited crosstalk with other phytohormones and transcription factors, indicating a regulatory network for jujube fruit ripening.
Conclusions
Our study further elucidated ABA-associated metabolic and regulatory processes. These findings are helpful for improving strategies for jujube fruit storage and for gaining insights into understand complex non-climacteric fruit ripening processes.
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Background
Chinese jujube (Ziziphus jujuba Mill.) is a popular fruit crop species that is native to China and is highly desired by consumers worldwide due to the abundant nutritional and health benefits of the fruit [1, 2]. However, the flesh jujube fruit has a very short shelf-life underlined by rapid dehydration or water-soaking deterioration within 2–3 days after harvest [3]. Therefore, fruit storage and quality maintenance have been among the most urgent challenges in the development of the jujube industry, whereas knowledge related to its ripening characterization and regulation is lacking. Over the past few decades, great strides have been made in elucidating the regulation of fruit ripening [4]; in particular, ethylene and abscisic acid (ABA) are recognized as the most important phytohormones that are directly or indirectly involved in the ripening of both climacteric and non-climacteric fruit [5, 6]. Recently, Chinese jujube has been characterized as a non-climacteric fruit, while a basal level of ethylene is still needed to maintain full fruit maturity [7]. These findings also reveal that the regulation of ripening is relatively complex and that there is a further need to explore these mechanisms to deepen our understanding of the ripening of Chinese jujube fruit.
With regard to ABA, the presence of dramatically increased levels in fruit during the onset of ripening has been reported in several fruit crop species, including grape [8], sweet cherry [9], cucumber [10], watermelon [11], and persimmon [5], which points to a role for ABA in triggering the onset of fruit ripening [8]. Moreover, applications of exogenous ABA and nordihydroguaiaretic acid (NDGA, an inhibitor of ABA biosynthesis) have enabled us to identify ABA-dependent pathways [12, 13]; increased numbers of research findings have suggested a positive role for ABA in promoting the metabolism and accumulation of soluble sugars [12, 14], formation of peel color [15, 16], and modification of cell wall catabolism [17], thereby accelerating ripening processes [5]. Fruit ripening is a highly integrated process that involves hormone control and crosstalk, as well as alterations to the numbers of transcripts of transcription factors (TFs) [61]. In the starch biosynthesis pathway, genes encoding ADP-glucose pyrophosphorylase and isoamylase were downregulated by ABA, while NDGA downregulated the expression of genes controlling starch degradation, including two alpha-amylase- and a beta-amylase-encoding genes. These results suggested that ABA was involved in starch metabolism, just as ZmEREB156 positively modulated starch biosynthesis via the synergistic effect of sucrose and ABA in maize [85]. For identification of differentially expressed genes (DEGs), an edgeR program [86] in OmicShare tools, a free online platform for data analysis (http://www.omicshare.com/tools), was used with a fold change (FC) threshold ≥2 and an false discovery rate (FDR) ≤ 0.05. The use of edgeR allowed comparative analysis within two replicates, and it had been used in several previous papers [12, 87, 88]. The functional enrichment of DEGs was determined using Gene Ontology (GO) and pathway analysis tools within the OmicShare platform [89]. We also used MapMan 3.6.0RC1 software to enrich the putative functional annotation of the DEGs [90, 91].
Quantitative real-time PCR validation for transcriptome expression levels
Total RNA was extracted using a plant RNA extraction kit (TaKaRa), and 200 ng of high-quality RNA was subsequently prepared for first-strand cDNA synthesis using a PrimeScript RT reagent kit with gDNA Eraser (TaKaRa). qPCR was then performed using a SYBR Premix Ex Taq II kit (TaKaRa) with a total volume of 10 μL, which comprised 1.0 μL of cDNA, 5.0 μL of SYBR premix solution, 0.4 μL of forward/reverse primers and 3.2 μL of dH2O. The thermal program for qPCR in a Roche LightCycler 96 system was set using the following conditions: 95 °C for 30 s; 40 cycles of amplification of 5 s at 95 °C, 30 s at 58 °C, and 30 s at 72 °C; and a default dissociation stage. The relative expression of each gene was normalized to that of a reference gene, ZjUBQ (Zhang et al. 2015), and was ultimately calculated using the 2-△Ct method (Livak and Schmittgen 2001). Sequences of the primers used for qPCR are listed in Additional file 10.
Statistical analysis
Statistical analysis was performed using the Duncan multiple range test (MRT) at the p < 0.05 level in SPSS 19.0. The error bars in the figures represent the standard deviations of three biological replicates.
Abbreviations
- AAO:
-
Abscisic aldehyde oxidase
- ABA:
-
Abscisic acid
- ABA2:
-
xanthoxin dehydrogenase
- ABA3:
-
molybdenum cofactor sulfurtransferase
- ACO:
-
1-aminocyclopropane-1-carboxylate oxidase
- ACS:
-
1-aminocyclopropane-1-carboxylate synthase
- AHP:
-
histidine-containing phosphotransferase
- AOG:
-
ABA-glucosyltransferase
- AP2/ERF:
-
APETALA2/ethylene-responsive element
- BG:
-
Beta-glucosidase
- BR:
-
Beginning red
- CYP707A:
-
ABA-8′-hydraxylase
- DAB:
-
Day after blooming
- DAT:
-
Day after treatment
- DEG:
-
Differentially expressed gene
- E:
-
Enlarging fruit
- EBF:
-
Ethylene insensitive 3-binding F-box
- EIN3/EIL:
-
Ethylene insensitive 3-like
- ERS:
-
Ethylene response
- ETR:
-
Ethylene receptor
- FC:
-
Fold change
- FDR:
-
False discovery rate
- FR:
-
Full-red
- GA:
-
Gibberenllin
- GA20ox:
-
GA-20-oxidase
- GA2ox:
-
GA-2-oxidase
- GH3:
-
Gretchen hagen 3
- GO:
-
Gene ontology
- HB:
-
Homeobox transcription factor
- HR:
-
Half-red
- HSF:
-
Heat-shock transcription factor
- KAO:
-
ent-kaurenoic acid hydroxylase
- LOG:
-
cytokinin riboside 5′-monophosphate phosphoribohydrolase
- MRT:
-
Multiple range test
- NCED:
-
Nine-cis-epoxycarotenoid dioxygenase
- NDGA:
-
Nordihydroguaiaretic acid
- PP2C:
-
Protein phosphatase 2C
- PYR/PYL/RCAR:
-
Pyrabatin resistance/pyrabatin resistance 1-like/regulatory component
- SnRK2:
-
Sucrose nonfermenting 1-related protein kinase 2
- TAA:
-
Tryptophan aminotransferase
- TF:
-
Transcription factor
- WM:
-
White mature
- YF:
-
Young fruit
- ZEP:
-
Zeaxanthin epoxidase
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This work was financially supported by the National Key R&D Program of China (2018YFD1000607), Ministry of Science and Technology of the People’s Republic of China. The supporters did not play any role in the design, collection, analysis, interpretation of the relevant data, or in writing the manuscript.
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ZZ and XL conceived and designed the experiments. ZZ performed samples preparation and conducted all the experiments, data analyses and wrote the manuscript. CK and SZ participated in determination of fruit respiration and ethylene production during postharvest storage. ZZ and XL contributed to the discussion. All authors approved the final manuscript.
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Additional files
Additional file 1:
Statistic information of RNA-seq data. (XLSX 11 kb)
Additional file 2:
Statistic information of map** data. (XLSX 11 kb)
Additional file 3:
GO enrichment for DEGs at DAT1. (XLSX 17 kb)
Additional file 4:
KEGG pathway enrichment for DEGs (Level3) at DAT1. (XLSX 27 kb)
Additional file 5:
DEGs related to metabolism pathways by MapMan. (XLSX 68 kb)
Additional file 6:
DEGs related to hormone metabolism and signaling. (XLSX 21 kb)
Additional file 7:
DEGs related to transcription factors involved in ripening regulation. (XLSX 27 kb)
Additional file 8:
RT-qPCR validation of digital expression patterns revealed by RNA sequencing. A number of 17 genes were selected to validate the transcriptomic expressions by qPCR. The correlation coefficient between the RNA-seq data and relative expression ranged from 0.838–1.0, thereby confirming the reliability of the RNA data. (DOCX 241 kb)
Additional file 9:
Phylogenetic analyses for NCED, CYP707A, BG, PYR/PYL/RCAR, PP2C, and SnRK2 genes. The trees were generated by the multiple alignments with putative proteins from Arabidopsis, grape, and tomato which were uploaded in the KEGG database using MEGA 7.0. The Bootstrap value was set into 1000 (Kumar et al. 2016). (DOCX 983 kb)
Additional file 10:
Sequences for ABA pathway genes. (XLSX 124 kb)
Additional file 11:
Accession of clean reads submitted to sequence read archives (SRA) of NCBI. (XLSX 10 kb)
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Zhang, Z., Kang, C., Zhang, S. et al. Transcript analyses reveal a comprehensive role of abscisic acid in modulating fruit ripening in Chinese jujube. BMC Plant Biol 19, 189 (2019). https://doi.org/10.1186/s12870-019-1802-2
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DOI: https://doi.org/10.1186/s12870-019-1802-2